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Title: The Kinetics of Electron Transfer from CdS Nanorods to the MoFe Protein of Nitrogenase

Abstract

Combining the remarkable catalytic properties of redox enzymes with highly tunable light absorbing properties of semiconductor nanocrystals enables the light-driven catalysis of complex, multielectron redox reactions. This work focuses on systems that combine CdS nanorods (NRs) with the MoFe protein of nitrogenase to drive photochemical N2 reduction. We used transient absorption spectroscopy (TAS) to examine the kinetics of electron transfer (ET) from CdS NRs to the MoFe protein. For CdS NRs with dimensions similar to those previously used for photochemical N2 reduction, the rate constant for ET from CdS NRs competes with other electron relaxation processes, such that when a MoFe protein is bound to a NR, about one-half of the photoexcited electrons are delivered to the enzyme. The NR-MoFe protein binding is incomplete with more than one-half of the NRs in solution not having a MoFe protein bound to accept electrons. The quantum efficiency of ET (QEET) in these ensemble samples is similar to previously reported efficiencies of product (NH3 and H2) formation, suggesting that the enzyme utilizes the delivered electrons without major loss pathways. Our analysis suggests that QEET, and therefore the photochemical product formation, is limited at the ensemble level by the NR-MoFe protein binding and atmore » the single-complex level by the competitiveness of ET. We characterized ET kinetics for several CdS NRs samples with varying dimensions and found that for CdS NRs with an average diameter of 4.2 nm the ET efficiency dropped to undetectable levels, defining a maximum NR diameter that should be used to photochemically drive the MoFe protein. The work described here provides insights into the design of systems with increased control of photochemical N2 reduction catalyzed by the MoFe protein of nitrogenase.« less

Authors:
 [1]; ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [1]; ORCiD logo [3]; ORCiD logo [4]; ORCiD logo [4]; ORCiD logo [5]; ORCiD logo [6]; ORCiD logo [2]; ORCiD logo [1]
  1. Univ. of Colorado, Boulder, CO (United States)
  2. Utah State Univ., Logan, UT (United States)
  3. Washington State Univ., Pullman, WA (United States); Montana State Univ., Bozeman, MT (United States)
  4. National Renewable Energy Lab. (NREL), Golden, CO (United States)
  5. Washington State Univ., Pullman, WA (United States)
  6. National Renewable Energy Lab. (NREL), Golden, CO (United States); Univ. of Colorado, Boulder, CO (United States)
Publication Date:
Research Org.:
National Renewable Energy Lab. (NREL), Golden, CO (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division; National Science Foundation (NSF)
OSTI Identifier:
1872406
Report Number(s):
NREL/JA-2700-81982
Journal ID: ISSN 1932-7447; MainId:82755;UUID:5e9c4e30-8394-4359-8e7a-fa288a6e0594;MainAdminID:64669
Grant/Contract Number:  
AC36-08GO28308; CHE-2125978
Resource Type:
Accepted Manuscript
Journal Name:
Journal of Physical Chemistry. C
Additional Journal Information:
Journal Volume: 126; Journal Issue: 19; Journal ID: ISSN 1932-7447
Publisher:
American Chemical Society
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; ammonia production; biohybrid; electron transfer; nanocrystal; solar fuels

Citation Formats

Ruzicka, Jesse L., Pellows, Lauren M., Kallas, Hayden, Shulenberger, Katherine E., Zadvornyy, Oleg A., Chica, Bryant, Brown, Katherine A., Peters, John W., King, Paul W., Seefeldt, Lance C., and Dukovic, Gordana. The Kinetics of Electron Transfer from CdS Nanorods to the MoFe Protein of Nitrogenase. United States: N. p., 2022. Web. doi:10.1021/acs.jpcc.2c02528.
Ruzicka, Jesse L., Pellows, Lauren M., Kallas, Hayden, Shulenberger, Katherine E., Zadvornyy, Oleg A., Chica, Bryant, Brown, Katherine A., Peters, John W., King, Paul W., Seefeldt, Lance C., & Dukovic, Gordana. The Kinetics of Electron Transfer from CdS Nanorods to the MoFe Protein of Nitrogenase. United States. https://doi.org/10.1021/acs.jpcc.2c02528
Ruzicka, Jesse L., Pellows, Lauren M., Kallas, Hayden, Shulenberger, Katherine E., Zadvornyy, Oleg A., Chica, Bryant, Brown, Katherine A., Peters, John W., King, Paul W., Seefeldt, Lance C., and Dukovic, Gordana. Mon . "The Kinetics of Electron Transfer from CdS Nanorods to the MoFe Protein of Nitrogenase". United States. https://doi.org/10.1021/acs.jpcc.2c02528. https://www.osti.gov/servlets/purl/1872406.
@article{osti_1872406,
title = {The Kinetics of Electron Transfer from CdS Nanorods to the MoFe Protein of Nitrogenase},
author = {Ruzicka, Jesse L. and Pellows, Lauren M. and Kallas, Hayden and Shulenberger, Katherine E. and Zadvornyy, Oleg A. and Chica, Bryant and Brown, Katherine A. and Peters, John W. and King, Paul W. and Seefeldt, Lance C. and Dukovic, Gordana},
abstractNote = {Combining the remarkable catalytic properties of redox enzymes with highly tunable light absorbing properties of semiconductor nanocrystals enables the light-driven catalysis of complex, multielectron redox reactions. This work focuses on systems that combine CdS nanorods (NRs) with the MoFe protein of nitrogenase to drive photochemical N2 reduction. We used transient absorption spectroscopy (TAS) to examine the kinetics of electron transfer (ET) from CdS NRs to the MoFe protein. For CdS NRs with dimensions similar to those previously used for photochemical N2 reduction, the rate constant for ET from CdS NRs competes with other electron relaxation processes, such that when a MoFe protein is bound to a NR, about one-half of the photoexcited electrons are delivered to the enzyme. The NR-MoFe protein binding is incomplete with more than one-half of the NRs in solution not having a MoFe protein bound to accept electrons. The quantum efficiency of ET (QEET) in these ensemble samples is similar to previously reported efficiencies of product (NH3 and H2) formation, suggesting that the enzyme utilizes the delivered electrons without major loss pathways. Our analysis suggests that QEET, and therefore the photochemical product formation, is limited at the ensemble level by the NR-MoFe protein binding and at the single-complex level by the competitiveness of ET. We characterized ET kinetics for several CdS NRs samples with varying dimensions and found that for CdS NRs with an average diameter of 4.2 nm the ET efficiency dropped to undetectable levels, defining a maximum NR diameter that should be used to photochemically drive the MoFe protein. The work described here provides insights into the design of systems with increased control of photochemical N2 reduction catalyzed by the MoFe protein of nitrogenase.},
doi = {10.1021/acs.jpcc.2c02528},
journal = {Journal of Physical Chemistry. C},
number = 19,
volume = 126,
place = {United States},
year = {2022},
month = {5}
}

Works referenced in this record:

Ligand Effects on Optical Properties of CdSe Nanocrystals
journal, April 2005

  • Kalyuzhny, Gregory; Murray, Royce W.
  • The Journal of Physical Chemistry B, Vol. 109, Issue 15
  • DOI: 10.1021/jp045352x

Quantum Efficiency of Charge Transfer Competing against Nonexponential Processes: The Case of Electron Transfer from CdS Nanorods to Hydrogenase
journal, December 2018

  • Utterback, James K.; Wilker, Molly B.; Mulder, David W.
  • The Journal of Physical Chemistry C, Vol. 123, Issue 1
  • DOI: 10.1021/acs.jpcc.8b09916

DLS and zeta potential – What they are and what they are not?
journal, August 2016


Diameter Dependent Electron Transfer Kinetics in Semiconductor–Enzyme Complexes
journal, October 2014

  • Brown, Katherine A.; Song, Qing; Mulder, David W.
  • ACS Nano, Vol. 8, Issue 10
  • DOI: 10.1021/nn504561v

Defining Intermediates of Nitrogenase MoFe Protein during N 2 Reduction under Photochemical Electron Delivery from CdS Quantum Dots
journal, July 2020

  • Chica, Bryant; Ruzicka, Jesse; Kallas, Hayden
  • Journal of the American Chemical Society, Vol. 142, Issue 33
  • DOI: 10.1021/jacs.0c06343

Catalytic and Biophysical Properties of a Nitrogenase Apo-MoFe Protein Produced by a n ifB -Deletion Mutant of Azotobacter v inelandii
journal, September 1998

  • Christiansen, Jason; Goodwin, Paul J.; Lanzilotta, William N.
  • Biochemistry, Vol. 37, Issue 36
  • DOI: 10.1021/bi981165b

Experimental Determination of the Extinction Coefficient of CdTe, CdSe, and CdS Nanocrystals
journal, July 2003

  • Yu, W. William; Qu, Lianhua; Guo, Wenzhuo
  • Chemistry of Materials, Vol. 15, Issue 14, p. 2854-2860
  • DOI: 10.1021/cm034081k

Nitrogenase Bioelectrocatalysis: ATP-Independent Ammonia Production Using a Redox Polymer/MoFe Protein System
journal, June 2020


Nitrogenase MoFe-Protein at 1.16 A Resolution: A Central Ligand in the FeMo-Cofactor
journal, September 2002


Spectroscopic Evidence for the Contribution of Holes to the Bleach of Cd-Chalcogenide Quantum Dots
journal, March 2019


Infrared spectroscopy of the nitrogenase MoFe protein under electrochemical control: potential-triggered CO binding
journal, January 2017

  • Paengnakorn, P.; Ash, P. A.; Shaw, S.
  • Chemical Science, Vol. 8, Issue 2
  • DOI: 10.1039/C6SC02860H

Nature of biological electron transfer
journal, February 1992

  • Moser, Christopher C.; Keske, Jonathan M.; Warncke, Kurt
  • Nature, Vol. 355, Issue 6363
  • DOI: 10.1038/355796a0

Light-driven carbon−carbon bond formation via CO 2 reduction catalyzed by complexes of CdS nanorods and a 2-oxoacid oxidoreductase
journal, December 2019

  • Hamby, Hayden; Li, Bin; Shinopoulos, Katherine E.
  • Proceedings of the National Academy of Sciences, Vol. 117, Issue 1
  • DOI: 10.1073/pnas.1903948116

Observation of trapped-hole diffusion on the surfaces of CdS nanorods
journal, July 2016

  • Utterback, James K.; Grennell, Amanda N.; Wilker, Molly B.
  • Nature Chemistry, Vol. 8, Issue 11
  • DOI: 10.1038/nchem.2566

Mechanism of Nitrogen Fixation by Nitrogenase: The Next Stage
journal, January 2014

  • Hoffman, Brian M.; Lukoyanov, Dmitriy; Yang, Zhi-Yong
  • Chemical Reviews, Vol. 114, Issue 8
  • DOI: 10.1021/cr400641x

Crystallographic structure of the nitrogenase iron protein from Azotobacter vinelandii
journal, September 1992


Natural engineering principles of electron tunnelling in biological oxidation–reduction
journal, November 1999

  • Page, Christopher C.; Moser, Christopher C.; Chen, Xiaoxi
  • Nature, Vol. 402, Issue 6757
  • DOI: 10.1038/46972

Balancing electron transfer rate and driving force for efficient photocatalytic hydrogen production in CdSe/CdS nanorod–[NiFe] hydrogenase assemblies
journal, January 2017

  • Chica, Bryant; Wu, Chang-Hao; Liu, Yuhgene
  • Energy & Environmental Science, Vol. 10, Issue 10
  • DOI: 10.1039/C7EE01738C

Electron Transfer from Semiconductor Nanocrystals to Redox Enzymes
journal, April 2020


Tailoring electron transfer pathway for photocatalytic N 2 -to-NH 3 reduction in a CdS quantum dots-nitrogenase system
journal, January 2022

  • Badalyan, Artavazd; Yang, Zhi-Yong; Hu, Maowei
  • Sustainable Energy & Fuels, Vol. 6, Issue 9
  • DOI: 10.1039/D2SE00148A

Temperature-Dependent Transient Absorption Spectroscopy Elucidates Trapped-Hole Dynamics in CdS and CdSe Nanorods
journal, May 2019

  • Utterback, James K.; Ruzicka, Jesse L.; Hamby, Hayden
  • The Journal of Physical Chemistry Letters, Vol. 10, Issue 11
  • DOI: 10.1021/acs.jpclett.9b00764

Investigating Protein–Nanocrystal Interactions for Photodriven Activity
journal, January 2020

  • Harris, Alexander W.; Harguindey, Albert; Patalano, Ryan E.
  • ACS Applied Bio Materials, Vol. 3, Issue 2
  • DOI: 10.1021/acsabm.9b01025

Characterization of Photochemical Processes for H 2 Production by CdS Nanorod–[FeFe] Hydrogenase Complexes
journal, March 2012

  • Brown, Katherine A.; Wilker, Molly B.; Boehm, Marko
  • Journal of the American Chemical Society, Vol. 134, Issue 12
  • DOI: 10.1021/ja2116348

On the Origin of Surface Traps in Colloidal II–VI Semiconductor Nanocrystals
journal, January 2017


Excitation-Rate Determines Product Stoichiometry in Photochemical Ammonia Production by CdS Quantum Dot-Nitrogenase MoFe Protein Complexes
journal, September 2020


Competition between electron transfer, trapping, and recombination in CdS nanorod–hydrogenase complexes
journal, January 2015

  • Utterback, James K.; Wilker, Molly B.; Brown, Katherine A.
  • Physical Chemistry Chemical Physics, Vol. 17, Issue 8
  • DOI: 10.1039/C4CP05993J

Large-scale purification of high activity Azotobacter vinelandii nitrogenase
journal, July 1980

  • Burgess, Barbara K.; Jacobs, Deloria B.; Stiefel, Edward I.
  • Biochimica et Biophysica Acta (BBA) - Enzymology, Vol. 614, Issue 1
  • DOI: 10.1016/0005-2744(80)90180-1

Electron Transfer within Nitrogenase: Evidence for a Deficit-Spending Mechanism
journal, November 2011

  • Danyal, Karamatullah; Dean, Dennis R.; Hoffman, Brian M.
  • Biochemistry, Vol. 50, Issue 43
  • DOI: 10.1021/bi201003a

NIH Image to ImageJ: 25 years of image analysis
journal, June 2012

  • Schneider, Caroline A.; Rasband, Wayne S.; Eliceiri, Kevin W.
  • Nature Methods, Vol. 9, Issue 7
  • DOI: 10.1038/nmeth.2089

ATP- and Iron−Protein-Independent Activation of Nitrogenase Catalysis by Light
journal, October 2010

  • Roth, Lauren E.; Nguyen, Joey C.; Tezcan, F. Akif
  • Journal of the American Chemical Society, Vol. 132, Issue 39
  • DOI: 10.1021/ja1071866

ATP-Uncoupled, Six-Electron Photoreduction of Hydrogen Cyanide to Methane by the Molybdenum–Iron Protein
journal, May 2012

  • Roth, Lauren E.; Tezcan, F. Akif
  • Journal of the American Chemical Society, Vol. 134, Issue 20
  • DOI: 10.1021/ja303265m

Electronic landscape of the P-cluster of nitrogenase as revealed through many-electron quantum wavefunction simulations
journal, September 2019


Linking surface chemistry to optical properties of semiconductor nanocrystals
journal, January 2015

  • Krause, Michael M.; Kambhampati, Patanjali
  • Physical Chemistry Chemical Physics, Vol. 17, Issue 29
  • DOI: 10.1039/C5CP02173A

Long-range electron transfer
journal, February 2005

  • Gray, H. B.; Winkler, J. R.
  • Proceedings of the National Academy of Sciences, Vol. 102, Issue 10
  • DOI: 10.1073/pnas.0408029102

Nitrogenase bioelectrocatalysis: heterogeneous ammonia and hydrogen production by MoFe protein
journal, January 2016

  • Milton, Ross D.; Abdellaoui, Sofiene; Khadka, Nimesh
  • Energy & Environmental Science, Vol. 9, Issue 8
  • DOI: 10.1039/C6EE01432A

Ligand Exchange and the Stoichiometry of Metal Chalcogenide Nanocrystals: Spectroscopic Observation of Facile Metal-Carboxylate Displacement and Binding
journal, November 2013

  • Anderson, Nicholas C.; Hendricks, Mark P.; Choi, Joshua J.
  • Journal of the American Chemical Society, Vol. 135, Issue 49, p. 18536-18548
  • DOI: 10.1021/ja4086758

Cluster-Dependent Charge-Transfer Dynamics in Iron–Sulfur Proteins
journal, January 2018


The surface science of nanocrystals
journal, January 2016

  • Boles, Michael A.; Ling, Daishun; Hyeon, Taeghwan
  • Nature Materials, Vol. 15, Issue 2
  • DOI: 10.1038/nmat4526

Substrate Interactions with the Nitrogenase Active Site
journal, March 2005

  • Dos Santos, Patricia C.; Igarashi, Robert Y.; Lee, Hong-In
  • Accounts of Chemical Research, Vol. 38, Issue 3
  • DOI: 10.1021/ar040050z

Activation Thermodynamics and H/D Kinetic Isotope Effect of the H ox to H red H + Transition in [FeFe] Hydrogenase
journal, September 2017

  • Ratzloff, Michael W.; Wilker, Molly B.; Mulder, David W.
  • Journal of the American Chemical Society, Vol. 139, Issue 37
  • DOI: 10.1021/jacs.7b04216

Electron Transfer in Nitrogenase
journal, January 2020


Establishing a Thermodynamic Landscape for the Active Site of Mo-Dependent Nitrogenase
journal, October 2019

  • Hickey, David P.; Cai, Rong; Yang, Zhi-Yong
  • Journal of the American Chemical Society, Vol. 141, Issue 43
  • DOI: 10.1021/jacs.9b06546

Mechanism of Mo-Dependent Nitrogenase
journal, June 2009


Nitrogenase Bioelectrochemistry for Synthesis Applications
journal, November 2019


Robust Photogeneration of H2 in Water Using Semiconductor Nanocrystals and a Nickel Catalyst
journal, November 2012


Controlled Assembly of Hydrogenase-CdTe Nanocrystal Hybrids for Solar Hydrogen Production
journal, July 2010

  • Brown, Katherine A.; Dayal, Smita; Ai, Xin
  • Journal of the American Chemical Society, Vol. 132, Issue 28
  • DOI: 10.1021/ja101031r

Role of Surface-Capping Ligands in Photoexcited Electron Transfer between CdS Nanorods and [FeFe] Hydrogenase and the Subsequent H 2 Generation
journal, December 2017

  • Wilker, Molly B.; Utterback, James K.; Greene, Sophie
  • The Journal of Physical Chemistry C, Vol. 122, Issue 1
  • DOI: 10.1021/acs.jpcc.7b07229

Recent Progress in Photocatalysis Mediated by Colloidal II-VI Nanocrystals
journal, December 2012

  • Wilker, Molly B.; Schnitzenbaumer, Kyle J.; Dukovic, Gordana
  • Israel Journal of Chemistry, Vol. 52, Issue 11-12
  • DOI: 10.1002/ijch.201200073

Electron Transfer Kinetics in CdS Nanorod–[FeFe]-Hydrogenase Complexes and Implications for Photochemical H 2 Generation
journal, March 2014

  • Wilker, Molly B.; Shinopoulos, Katherine E.; Brown, Katherine A.
  • Journal of the American Chemical Society, Vol. 136, Issue 11
  • DOI: 10.1021/ja413001p

Synthesis and enzymatic photo-activity of an O 2 tolerant hydrogenase–CdSe@CdS quantum rod bioconjugate
journal, January 2014

  • Hamon, C.; Ciaccafava, A.; Infossi, P.
  • Chem. Commun., Vol. 50, Issue 39
  • DOI: 10.1039/C3CC49368G

Improvements to the APBS biomolecular solvation software suite: Improvements to the APBS Software Suite
journal, October 2017

  • Jurrus, Elizabeth; Engel, Dave; Star, Keith
  • Protein Science, Vol. 27, Issue 1
  • DOI: 10.1002/pro.3280

CONTIN: A general purpose constrained regularization program for inverting noisy linear algebraic and integral equations
journal, September 1982


Relationships between Exciton Dissociation and Slow Recombination within ZnSe/CdS and CdSe/CdS Dot-in-Rod Heterostructures
journal, May 2017


Effect of Surface Ligands on Optical and Electronic Spectra of Semiconductor Nanoclusters
journal, June 2009

  • Kilina, Svetlana; Ivanov, Sergei; Tretiak, Sergei
  • Journal of the American Chemical Society, Vol. 131, Issue 22
  • DOI: 10.1021/ja9005749

Chemistry and Properties of Nanocrystals of Different Shapes
journal, April 2005

  • Burda, Clemens; Chen, Xiaobo; Narayanan, Radha
  • Chemical Reviews, Vol. 105, Issue 4
  • DOI: 10.1021/cr030063a

The Role of Ligands in Determining the Exciton Relaxation Dynamics in Semiconductor Quantum Dots
journal, April 2014


Multigrid solution of the Poisson?Boltzmann equation
journal, January 1993

  • Holst, Michael; Saied, Faisal
  • Journal of Computational Chemistry, Vol. 14, Issue 1
  • DOI: 10.1002/jcc.540140114

Substrate Interaction at an Iron-Sulfur Face of the FeMo-cofactor during Nitrogenase Catalysis
journal, October 2004

  • Barney, Brett M.; Igarashi, Robert Y.; Dos Santos, Patricia C.
  • Journal of Biological Chemistry, Vol. 279, Issue 51
  • DOI: 10.1074/jbc.M410247200

Avogadro: an advanced semantic chemical editor, visualization, and analysis platform
journal, August 2012

  • Hanwell, Marcus D.; Curtis, Donald E.; Lonie, David C.
  • Journal of Cheminformatics, Vol. 4, Issue 1
  • DOI: 10.1186/1758-2946-4-17

Charge Transfer Dynamics between Photoexcited CdS Nanorods and Mononuclear Ru Water-Oxidation Catalysts
journal, February 2013

  • Tseng, Huan-Wei; Wilker, Molly B.; Damrauer, Niels H.
  • Journal of the American Chemical Society, Vol. 135, Issue 9
  • DOI: 10.1021/ja400178g

Mechanism of Molybdenum Nitrogenase
journal, January 1996

  • Burgess, Barbara K.; Lowe, David J.
  • Chemical Reviews, Vol. 96, Issue 7
  • DOI: 10.1021/cr950055x

The coordination chemistry of nanocrystal surfaces
journal, February 2015


Numerical solution of the nonlinear Poisson-Boltzmann equation: Developing more robust and efficient methods
journal, March 1995

  • Holst, Michael J.; Saied, Faisal
  • Journal of Computational Chemistry, Vol. 16, Issue 3
  • DOI: 10.1002/jcc.540160308

Electron Transfer from the Nitrogenase Iron Protein to the [8Fe-(7/8)S] Clusters of the Molybdenum−Iron Protein
journal, January 1996

  • Lanzilotta, William N.; Seefeldt, Lance C.
  • Biochemistry, Vol. 35, Issue 51
  • DOI: 10.1021/bi962286j

Light-driven dinitrogen reduction catalyzed by a CdS:nitrogenase MoFe protein biohybrid
journal, April 2016


Dissecting Electronic-Structural Transitions in the Nitrogenase MoFe Protein P-Cluster during Reduction
journal, March 2022

  • Chica, Bryant; Ruzicka, Jesse; Pellows, Lauren M.
  • Journal of the American Chemical Society, Vol. 144, Issue 13
  • DOI: 10.1021/jacs.1c13311

Nitrogenase Complexes: Multiple Docking Sites for a Nucleotide Switch Protein
journal, August 2005


Exciton Localization and Dissociation Dynamics in CdS and CdS–Pt Quantum Confined Nanorods: Effect of Nonuniform Rod Diameters
journal, July 2014

  • Wu, Kaifeng; Rodríguez-Córdoba, William; Lian, Tianquan
  • The Journal of Physical Chemistry B, Vol. 118, Issue 49
  • DOI: 10.1021/jp504703t

Reduction of Substrates by Nitrogenases
journal, March 2020